Gastrointestinal microbiome of ARDS patients induces neuroinflammation and cognitive impairment in mice
Abstract Background Acute respiratory distress syndrome (ARDS) is a respiratory failure syndrome that can cause many complications, impacting patients’ quality of life. Behavioral and cognitive disorders have attracted increasing attention in patients with ARDS, but its potential mechanisms are stil...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-07-01
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| Series: | Journal of Neuroinflammation |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12974-023-02825-7 |
| _version_ | 1797778755858464768 |
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| author | Hong Zheng Qihui Zhao Jianuo Chen Jiahui Lu Yuping Li Hongchang Gao |
| author_facet | Hong Zheng Qihui Zhao Jianuo Chen Jiahui Lu Yuping Li Hongchang Gao |
| author_sort | Hong Zheng |
| collection | DOAJ |
| description | Abstract Background Acute respiratory distress syndrome (ARDS) is a respiratory failure syndrome that can cause many complications, impacting patients’ quality of life. Behavioral and cognitive disorders have attracted increasing attention in patients with ARDS, but its potential mechanisms are still elusive. Methods Herein we transferred the faecal microbiota from patients with ARDS caused by community-acquired pneumonia (CAP) to antibiotics-treated recipient male mice to explore the microbiota-gut-brain mechanisms. Behavioral functions of mice were evaluated by the open field test, Morris water maze and Y-maze test. The structure and composition of the gut microbiota were analyzed by using 16S rRNA sequencing analysis. Microglia, astrocyte and neuron in the cortex and hippocampus were examined via immunofluorescent staining. Results We found that the major characteristic of the intestinal flora in ARDS/CAP patients was higher abundances of Gram-negative bacteria than normal controls. The gut microbiota derived from ARDS/CAP patients promoted neuroinflammation and behavioral dysfunctions in mice. Mice who underwent fecal transplant from ARDS/CAP patients had increased systemic lipopolysaccharide (LPS), systemic inflammation, and increased colonic barrier permeability. This may adversely impact blood barrier permeability and facilitate microglia activation, astrocyte proliferation, and loss of neurons. Conclusions Our study proposes the role of the microbiota-gut-brain crosstalk on ARDS/CAP-associated behavioral impairments and suggests the gut microbiota as a potential target for the protection of brain health in ARDS patients in clinical practice. |
| first_indexed | 2024-03-12T23:22:08Z |
| format | Article |
| id | doaj.art-455954cdf039446ba345d7b996d1793a |
| institution | Directory Open Access Journal |
| issn | 1742-2094 |
| language | English |
| last_indexed | 2024-03-12T23:22:08Z |
| publishDate | 2023-07-01 |
| publisher | BMC |
| record_format | Article |
| series | Journal of Neuroinflammation |
| spelling | doaj.art-455954cdf039446ba345d7b996d1793a2023-07-16T11:23:26ZengBMCJournal of Neuroinflammation1742-20942023-07-0120111410.1186/s12974-023-02825-7Gastrointestinal microbiome of ARDS patients induces neuroinflammation and cognitive impairment in miceHong Zheng0Qihui Zhao1Jianuo Chen2Jiahui Lu3Yuping Li4Hongchang Gao5Oujiang Laboratory, School of Pharmaceutical Sciences, Wenzhou Medical UniversityOujiang Laboratory, School of Pharmaceutical Sciences, Wenzhou Medical UniversityDepartment of Pulmonary and Critical Care Medicine, The First Affiliated Hospital of Wenzhou Medical UniversityOujiang Laboratory, School of Pharmaceutical Sciences, Wenzhou Medical UniversityDepartment of Pulmonary and Critical Care Medicine, The First Affiliated Hospital of Wenzhou Medical UniversityOujiang Laboratory, School of Pharmaceutical Sciences, Wenzhou Medical UniversityAbstract Background Acute respiratory distress syndrome (ARDS) is a respiratory failure syndrome that can cause many complications, impacting patients’ quality of life. Behavioral and cognitive disorders have attracted increasing attention in patients with ARDS, but its potential mechanisms are still elusive. Methods Herein we transferred the faecal microbiota from patients with ARDS caused by community-acquired pneumonia (CAP) to antibiotics-treated recipient male mice to explore the microbiota-gut-brain mechanisms. Behavioral functions of mice were evaluated by the open field test, Morris water maze and Y-maze test. The structure and composition of the gut microbiota were analyzed by using 16S rRNA sequencing analysis. Microglia, astrocyte and neuron in the cortex and hippocampus were examined via immunofluorescent staining. Results We found that the major characteristic of the intestinal flora in ARDS/CAP patients was higher abundances of Gram-negative bacteria than normal controls. The gut microbiota derived from ARDS/CAP patients promoted neuroinflammation and behavioral dysfunctions in mice. Mice who underwent fecal transplant from ARDS/CAP patients had increased systemic lipopolysaccharide (LPS), systemic inflammation, and increased colonic barrier permeability. This may adversely impact blood barrier permeability and facilitate microglia activation, astrocyte proliferation, and loss of neurons. Conclusions Our study proposes the role of the microbiota-gut-brain crosstalk on ARDS/CAP-associated behavioral impairments and suggests the gut microbiota as a potential target for the protection of brain health in ARDS patients in clinical practice.https://doi.org/10.1186/s12974-023-02825-7ARDSBehaviorGut-brain axisInflammationMicroglia |
| spellingShingle | Hong Zheng Qihui Zhao Jianuo Chen Jiahui Lu Yuping Li Hongchang Gao Gastrointestinal microbiome of ARDS patients induces neuroinflammation and cognitive impairment in mice Journal of Neuroinflammation ARDS Behavior Gut-brain axis Inflammation Microglia |
| title | Gastrointestinal microbiome of ARDS patients induces neuroinflammation and cognitive impairment in mice |
| title_full | Gastrointestinal microbiome of ARDS patients induces neuroinflammation and cognitive impairment in mice |
| title_fullStr | Gastrointestinal microbiome of ARDS patients induces neuroinflammation and cognitive impairment in mice |
| title_full_unstemmed | Gastrointestinal microbiome of ARDS patients induces neuroinflammation and cognitive impairment in mice |
| title_short | Gastrointestinal microbiome of ARDS patients induces neuroinflammation and cognitive impairment in mice |
| title_sort | gastrointestinal microbiome of ards patients induces neuroinflammation and cognitive impairment in mice |
| topic | ARDS Behavior Gut-brain axis Inflammation Microglia |
| url | https://doi.org/10.1186/s12974-023-02825-7 |
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